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A Novel Indigenous New World Monopartite Begomovirus Infecting Tomato in Venezuela

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A Novel Indigenous New World Monopartite Begomovirus Infecting Tomato in Venezuela viruses Communication Tomato Twisted Leaf Virus: A Novel Indigenous New World Monopartite Begomovirus Infecting Tomato in Venezuela Gustavo Romay 1,*, Francis Geraud-Pouey 2, Dorys T. Chirinos 3, Mathieu Mahillon 1, Annika Gillis 4,† , Jacques Mahillon 4 and Claude Bragard 1,* 1 UCLouvain, Earth and Life Institute, Applied Microbiology-Phytopathology, Croix du Sud 2-L07.05.03, 1348 Louvain-la-Neuve, Belgium; [email protected] 2 La Universidad del Zulia (LUZ), Unidad Técnica Fitosanitaria, Maracaibo 4005, Estado Zulia, Venezuela; [email protected] 3 Facultad de Ingeniería Agronómica, Universidad Técnica de Manabí, Manabí 130105, Ecuador; [email protected] 4 UCLouvain, Earth and Life Institute, Applied Microbiology-Laboratory of Food and Environmental Microbiology, Croix du Sud 2-L7.05.12, 1348 Louvain-la-Neuve, Belgium; [email protected] (A.G.); [email protected] (J.M.) * Correspondence: [email protected] (G.R.); [email protected] (C.B.) † Present address: Section of Microbiology and Medical Research Council Centre for Molecular Bacteriology and Infection, Imperial College London, London SW72AZ, UK. Received: 21 February 2019; Accepted: 2 April 2019; Published: 4 April 2019 Abstract: Begomoviruses are one of the major groups of plant viruses with an important economic impact on crop production in tropical and subtropical regions. The global spread of its polyphagous vector, the whitefly Bemisia tabaci, has contributed to the emergence and diversification of species within this genus. In this study, we found a putative novel begomovirus infecting tomato plants in Venezuela without a cognate DNA-B component. This begomovirus was genetically characterized and compared with related species. Furthermore, its infectivity was demonstrated by agroinoculation of infectious clones in tomato (Solanum lycopersicum) and Nicotiana benthamiana plants. The name Tomato twisted leaf virus (ToTLV) is proposed. ToTLV showed the typical genome organization of the DNA-A component of New World bipartite begomoviruses. However, the single DNA component of ToTLV was able to develop systemic infection in tomato and N. benthamiana plants, suggesting a monopartite nature of its genome. Interestingly, an additional open reading frame ORF was observed in ToTLV encompassing the intergenic region and the coat protein gene, which is not present in other closely related begomoviruses. A putative transcript from this region was amplified by strand-specific reverse transcription-PCR. Along with recent studies, our results showed that the diversity of monopartite begomoviruses from the New World is greater than previously thought. Keywords: begomovirus evolution; Geminiviridae; Solanum lycopersicum; tomato crop 1. Introduction Over the course of the last few decades, members of the genus Begomovirus have remained serious threats to tomato production in tropical and subtropical regions across the world. Begomoviruses represent the largest group of plant viruses and belong to the family Geminiviridae along with members of eight different genera: Becurtovirus, Capulavirus, Curtovirus, Eragrovirus, Grablovirus, Mastrevirus, Topocuvirus, and Turncurtovirus [1]. One of the most important factors mediating the ever-increasing emergence and dissemination of begomoviruses is the global spread of its vector, the whitefly Bemisia Viruses 2019, 11, 327; doi:10.3390/v11040327 www.mdpi.com/journal/viruses Viruses 2019, 11, 327 2 of 11 tabaci [2]. The genome of begomoviruses has one or two circular single-stranded DNA components, referred to as DNA-A and DNA-B [3]. The DNA-A of bipartite begomoviruses is homologous to the genome of monopartite begomoviruses and encodes the capsid protein (open reading frame (ORF) AV1/V1), the AV2/V2 protein (ORF AV2/V2), the replication-associated protein (ORF AC1/C1), the transcriptional activator protein (ORF AC2/C2), the replication enhancer protein (ORF AC3/C3), and the AC4/C4 protein (ORF AC4/C4), while the DNA-B encodes the nuclear shuttle protein (ORF BV1) and the movement protein (ORF BC1) [1]. For taxonomical purposes, the full-length sequence of DNA-A, or its homologous DNA of monopartite begomoviruses, is used to classify and distinguish species into their begomovirus group considering 91% of nucleotide identity as the demarcation threshold [3]. Begomoviruses can be separated in two geographically distant groups, the New World (NW) group and the Old World (OW) group. In general, NW begomoviruses have a bipartite genome, while the majority of OW begomoviruses (ca. 85%) display a monopartite genome [2]. Both DNA-A and DNA-B components of bipartite begomoviruses are required for systemic infection [3]: while DNA-A is responsible for replication and transcription functions, DNA-B is implicated in the viral movement [4]. Unlike bipartite begomoviruses, only the single DNA component of monopartite begomoviruses is essential to develop systemic infection [4]. Another difference between both geographic groups is the lack of the AV2 gene in the genome of NW begomoviruses [1]. Although NW begomoviruses had been thought to have only bipartite genomes, a new tomato begomovirus containing a single DNA component was reported in Peru in 2011 [5]. This virus was named Tomato leaf deformation virus (ToLDeV) and its infectivity was demonstrated through development of several infectious clones [6,7]. In this study, a putative new begomovirus species infecting tomato plants was found in Venezuela containing a single DNA component. Further assays to fulfill Koch’s postulates were conducted with this novel virus and demonstrated the monopartite nature of its genome. 2. Materials and Methods 2.1. Sample Collection and Begomovirus Detection In July 2005, during a survey of begomoviruses carried out in Venezuela [8], leaf samples were collected in Zulia state from two tomato plants (samples 2005-07-22-01 and 2005-07-22-02; hereafter referred to as 331 and 332, respectively) exhibiting leaf deformation and stunting symptoms. Each sample was dried on a sealed receptacle containing Silicagel®. The dried samples were wrapped on tissue paper and stored in 2 mL tubes at −20 ◦C until use. Total DNA was extracted using a standard protocol [9] and PCR detection for begomoviruses was performed using the degenerate primer pairs PAL1v1978/PAR1c946 and PBLv2040/PCRc1 [10] and Taq DNA Polymerase master mix (New England BioLabs, USA). PCR conditions were as follows: 2 min at 94 ◦C, 35 cycles at 94, 55, and 68 ◦C for 30, 30, and 60 s, respectively, and a final extension of 5 min at 68 ◦C. PCR products were cloned in Escherichia coli competent cells using the pGem®-T Easy vector system (Promega, USA). At least five clones were sequenced for further BLAST analysis. 2.2. Cloning of Full-Length Viral Genomes Using tomato samples 331 and 332, a 1.1 kb fragment was cloned and subsequently sequenced. Since they shared 99.8% of identity, only sample 332 was considered for subsequent studies. DNA from this sample was used as a template to obtain the viral sequences by rolling circle amplification (RCA) using F29 DNA polymerase (TempliPhi, GE Healthcare, Munich, Germany). Restriction enzymes BamHI, EcoRI, HindIII, and PstI were used to follow a protocol of restriction fragment length polymorphism (RFLP) on RCA products (RFLP-RCA) according to Haible et al. [11]. The bands were excised from agarose gel and inserted into the appropriate restriction sites in pBluescript II SK (+) (La Jolla, Stratagene, CA, USA) for subsequent transformation of E. coli competent cells. Viruses 2019, 11, 327 3 of 11 The cloned products were sequenced at Macrogen Inc. (Amsterdam, Netherlands). A preliminary identification of viral sequences was based on a BLAST search and three different begomovirus DNA components were observed, suggesting a mixed infection. Subsequently, the three different full-length viral clones, referred to as isolates Be1.1B, Be6.6H, and B6.7H, were completely sequenced by primer walking and assembled using BioEdit v.7.1.9 [12]. The complete nucleotide sequence of clones Be6.6H, Be6.7H, and Be1.1B were deposited in GenBank under the accession numbers MK440292, MK440293, and MK440294, respectively. 2.3. Pairwise Identity, Phylogenetic, and Recombination Analyses Since the isolate Be6.6H did not show more than 90% of nucleotide identity with any begomovirus in GenBank database, it was considered for further genetic and biological studies. Isolate Be6.6H was aligned with sequences of related NW begomoviruses using MUSCLE [13] and pairwise sequence identities were estimated using the Sequence Demarcation Tool (SDT) v.1.2 [14]. The aligned sequences were analyzed to determine the optimal nucleotide substitution model and generate a maximum-likelihood phylogenetic tree (500 bootstrap replicates) using MEGA X v10.0.5 [15]. The phylogenetic tree was rooted with the OW begomovirus species African cassava mosaic virus (ACMV). In order to identify potential recombination events in isolate Be6.6H, putative parental begomoviruses were downloaded from GenBank based on sequence analysis with the software SWeBLAST [16]. These viruses were aligned to perform recombination analyses using the methods BoostScan, Chimera, GENCOV, MaxChi, RDP, SiScan, and 3Seq implemented in RDP4 software v.4.31 [17]. Only recombination events detected by at least five out of seven methods were considered. 2.4. Construction of an Infectious Clone of Isolate Be6.6H for Agroinoculation A cognate DNA-B component of the isolate Be6.6H was found neither by PCR with begomovirus
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